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Tiêu đề Curcumin Reduces Expression Of Bcl-2, Leading To Apoptosis In Daunorubicin-Insensitive CD34+ Acute Myeloid Leukemia Cell Lines And Primary Sorted CD34+ Acute Myeloid Leukemia Cells
Tác giả Jia Rao, Duo-Rong Xu, Fei-Meng Zheng, Zi-Jie Long, Sheng-Shan Huang, Xing Wu, Wei-Hua Zhou, Ren-Wei Huang, Quentin Liu
Trường học Sun Yat-sen University
Chuyên ngành Hematology
Thể loại báo cáo
Năm xuất bản 2011
Thành phố Guangzhou
Định dạng
Số trang 15
Dung lượng 1,9 MB

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Nội dung

The aim of this study was to therefore to explore curcumin-induced cytotoxicity in DNR-insensitive CD34+AML cell lines KG1a, Kasumi-1, DNR-sensitive U937 AML cells, and primary CD34+AML

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R E S E A R C H Open Access

Curcumin reduces expression of Bcl-2, leading to

acute myeloid leukemia cell lines and primary

Jia Rao1,2, Duo-Rong Xu2,3*, Fei-Meng Zheng4, Zi-Jie Long1,2, Sheng-Shan Huang5, Xing Wu1,2, Wei-Hua Zhou1,2, Ren-Wei Huang1,2*and Quentin Liu1,2,4*

Abstract

Background: Acute myeloid leukemia (AML) is an immunophenotypically heterogenous malignant disease, in which CD34 positivity is associated with poor prognosis CD34+AML cells are 10-15-fold more resistant to daunorubicin (DNR) than CD34-AML cells Curcumin is a major component of turmeric that has shown cytotoxic activity in

multiple cancers; however, its anti-cancer activity has not been well studied in DNR-insensitive CD34+AML cells The aim of this study was to therefore to explore curcumin-induced cytotoxicity in DNR-insensitive CD34+AML cell lines (KG1a, Kasumi-1), DNR-sensitive U937 AML cells, and primary CD34+AML bone-marrow-derived cells

Methods: Primary human CD34+cells were isolated from peripheral blood mononuclear cells or bone marrow mononuclear cells using a CD34 MicroBead kit The growth inhibitory effects of curcumin were evaluated by MTT and colony-formation assays Cell cycle distribution was examined by propidium iodide (PI) assay Apoptosis was analyzed by Wright-Giemsa, Hoechst 33342 and Annexin-V/PI staining assays The change in mitochondrial

membrane potential (MMP) was examined by JC-1 staining and flow cytometry Expression of apoptosis-related proteins was determined by reverse transcription-polymerase chain reaction and Western blotting Short interfering RNA (siRNA) against Bcl-2 was used in CD34+KG1a and Kasumi-1 cells incubated with/without DNR

Results: Curcumin inhibited proliferation and induced apoptosis and G1/S arrest in both DNR-insensitive KG1a, Kasumi-1 and DNR-sensitive U937 cells Curcumin-induced apoptosis was associated with reduced expression of both Bcl-2 mRNA and protein, subsequent loss of MMP, and activation of caspase-3 followed by PARP degradation Curcumin synergistically enhanced the cytotoxic effect of DNR in DNR-insensitive KG1a and Kasumi-1 cells,

consistent with decreased Bcl-2 expression Accordingly, siRNA against Bcl-2 increased the susceptibility of KG1a and Kasumi-1 cells to DNR-induced apoptosis More importantly, curcumin suppressed Bcl-2 expression, selectively inhibited proliferation and synergistically enhanced the cytotoxicity of DNR in primary CD34+AML cells, while showing limited lethality in normal CD34+hematopoietic progenitors

Conclusion: Curcumin down-regulates Bcl-2 and induces apoptosis in DNR-insensitive CD34+AML cell lines and primary CD34+AML cells

* Correspondence: xudr@hotmail.com; huangrw56@163.com; liuq9@mail.sysu.

edu.cn

1

Department of Hematology, Third Affiliated Hospital, Sun Yat-sen University,

600 Tianhe Road, Guangzhou 510630, P.R China

2

Sun Yat-sen Institute of Hematology, 600 Tianhe Road, Guangzhou 510630,

P.R China

Full list of author information is available at the end of the article

© 2011 Rao et al; licensee BioMed Central Ltd This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in

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Acute myeloid leukemia (AML) is an

immunophenotypi-cally heterogenous malignant disease, in which CD34

posi-tivity has been significantly correlated with a lower

complete response (CR) rate, drug resistance and poor

outcome [1-3] Treatment of AML has generally consisted

of a combination of cytarabine and an anthracycline such

as daunorubicin (DNR), or the anthracenedione

mitoxan-trone [4] Although conventional chemotherapy regimens

induce CR in 65-80% of newly diagnosed AML patients,

most patients who achieve a CR relapse within 2 years

from diagnosis [5] At relapse, blast cells usually display a

more immature phenotype, with one of the most common

antigenic changes being a gain in expression of the stem

cell antigen CD34 [6,7] This is reflected in the resistance

of these immature phenotype CD34+AML progenitors to

current chemotherapies

CD34+ AML cells are 10-15-fold more resistant to

DNR than CD34-AML cells [8] CD34+ KG1a and TF-1

AML cell lines are 30-40 fold more resistant to

mitox-antrone than more mature HL-60 and U937 cells, and

this resistance appears to be associated with the lack of

apoptosis [9] Increasing evidence indicates that CD34+

AML cells are less sensitive to spontaneous apoptosis

and have higher levels of Bcl-2 and Bcl-xl gene and

pro-tein expression than the CD34-subpopulation [6,10-12]

CD34 positivity has been reported to be another

indica-tor of poor prognosis in AML [3,12], and use of more

effective drugs to eliminate this early immature CD34+

AML cell subpopulation might therefore improve the

outcome of AML

DNR is one of the most commonly used anti-leukemia

agents Bcl-2 overexpression can block DNR-induced

apoptosis in more mature U937 AML cells [13] The

anti-apoptotic proteins Bcl-2 and Bcl-xl also contribute

to the survival and chemoresistance of quiescent

leuke-mia CD34+ cells [14] These findings suggest that Bcl-2

plays a critical role in CD34+AML cell survival and that

agents aimed at down-regulating Bcl-2 protein might be

effective for the treatment of DNR-insensitive CD34+

AML

Curcumin, a major yellow pigment in turmeric, has

been proven to be a powerful therapeutic drug [15,16]

Curcumin induces apoptosis in a variety of tumor cells,

including more mature HL-60 and U937 cell lines,

through activation of caspase-3, cytochrome c release,

and down-regulation of Bcl-2 [17-20] Curcumin inhibits

proliferation in a variety of cancer cells through

target-ing multiple cellular signaltarget-ing pathways [21], includtarget-ing

the mitogen-activated protein kinase [22], nuclear factor

kappaB [23], phosphoinositide-3 kinase/Akt/mammalian

target of rapamycin [24,25], Wnt [26], and

Notch-mediated signaling pathways [27] Curcumin has also

been found to be a powerful chemosensitizing agent in tumor cells It demonstrated no major toxicities in phase I and II clinical studies at doses of up to 8 g/day [28,29] However, the cytotoxic effects of curcumin in DNR-insensitive CD34+ immature AML cells remain unclear

In this study, we examined the cytotoxic efficiency and molecular mechanisms underlying the anticancer activity

of curcumin in both DNR-insensitive CD34+ immature AML cell lines and in primary CD34+AML cells

Methods

Materials Curcumin (Sigma, St Louis, MO) was dissolved in dimethyl sulfoxide (DMSO) to prepare a 100-mM stock solution that was stored at -20°C DNR was purchased from Pharmacia & Upjohn SpA (Milan, Italy) Annexin-V assay kit was purchased from Molecular Probes (Eugene,

OR, USA) Anti-cleaved PARP, cleaved caspase-3, and Bcl-2 antibodies were purchased from Cell Signaling Technologies (Beverly, MA, USA) Anti-GAPDH anti-body and goat anti-rabbit/mouse-horseradish peroxidase (HRP)-conjugated secondary antibody were purchased from Protein Tech Group (Chicago, IL, USA) JC-1 kit was purchased from Beyotime (China) CD34-PE and IgG1-PE monoclonal antibodies were purchased from BD Biosciences (San Jose, CA, USA) CD34 MicroBead kit was purchased from Miltenyi biotec (Auburn, CA, USA)

Cell lines, primary samples, and cell culture KG1a and Kasumi-1 cell lines were obtained from Deutsche Sammlung von Mikroorganismen und Zellkul-turen GmbH (DSMZ) (Braunschweig, Germany) and grown in RPMI 1640 medium (Gibco; Invitrogen, Carls-bad, CA, USA) supplemented with 20% (v/v) fetal bovine serum (FBS; Hyclone, Logan, UT) According to immu-nological studies by DSMZ and others [30,31], KG1a and Kasumi-1 cells are characterized by high expression of CD34 surface antigen U937 cells were obtained from the American Type Culture Collection (ATCC) and grown in RPMI 1640 medium supplemented with 10% FBS Cells were cultured at 37°C in a humidified atmosphere con-taining 5% CO2 Control cultures received an equivalent amount of DMSO only Bone marrow mononuclear cells (BMMCs) or mobilized peripheral blood mononuclear cells (PBMCs) were obtained from 9 newly diagnosed AML patients and 8 healthy donors All donors provided written informed consent, and the study had the approval

of the Institute Research Ethics Committee at Sun Yan-sen University, in accordance with the Declaration of Helsinki Patient characteristics are shown in Table 1 PBMCs and BMMCs were enriched by Ficoll-Hypaque density gradient centrifugation and isolated using a CD34

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MicroBead kit BMMCs and PBMCs were stained with

PE-conjugated anti-CD34 to determine the purity of

CD34+cells

MTT assay

Viability was assessed by MTT assay Briefly, 1.0×104

cells were incubated in triplicate in a 96-well plate in the

presence or absence of the indicated test samples in a

final volume of 0.2 ml for various lengths of time at 37°C

Thereafter, 20μl MTT solution (5 mg/ml in PBS) was

then added to each well After 4-h incubation at 37°C,

150μl DMSO was added Finally the plates were shaken

and the optical density at 490 nm was measured using a

multiwell plate reader (Microplate Reader; Bio-Rad,

Hercules, CA) Percent cell viability was calculated as cell

viability of the experimental samples/cell viability of the

control samples × 100 At least three independent

experi-ments were performed

Colony-forming assay

Treated and untreated cells were cultured in RPMI 1640

medium supplemented with 0.9% methylcellulose and

20% FBS at 37°C in 5% CO2 The colonies (containing

50 or more cells) were counted by light microscopy

after 14 days All semi-solid cultures were performed in

triplicate Three independent experiments were

performed

Wright-Giemsa staining

Morphological signs of apoptosis were detected by

Wright-Giemsa staining Cells were treated with 0-80μM

curcumin for 24 h Smears of control and treated cells

were stained with Wright-Giemsa solution for 25 min,

rinsed with distilled water and air dried Cell morphology

was studied by light microscopy

Hoechst 33342 staining

Nuclear fragmentation was examined by Hoechst 33342

(Sigma) Cells treated with 0-80μM curcumin for 24 h

were washed and stained with Hoechst 33342 (10μg/ml) for 15 min at 37°C Slides were viewed using a fluores-cence microscope

Measurement of apoptosis by Annexin V analysis

An Annexin V-binding assay was used according to the manufacturer’s instructions Briefly, approximately 5×105/ml cells in 6-well plates were treated with various concentrations of the indicated test samples The cells were harvested and used for Annexin V-Alexa Fluor-488/PI staining The stained cells were analyzed by flow cytometry to determine the percentages of AnnexinV

+

/PI-(early apoptosis) and AnnexinV+/PI+ (late apopto-sis) cells

Cell cycle analysis Cell cycle was analyzed by flow cytometry Approxi-mately 5 × 105/ml cells in 6-well plates were treated with various concentrations of curcumin for 24 h Cell cycle analysis was performed using the CycleTEST™ PLUS DNA kit (BD Biosciences)

Detection of mitochondrial membrane potential (MMP, Δψm) using JC-1

MMP was estimated by flow cytometry after staining with JC-1 fluorescent dye When the cell is in a normal state, MMP is high and JC-1 predominantly appears as red fluorescence When the cell is in an apoptotic or necrotic state, the MMP is reduced and JC-1 appears as a monomer indicated by green fluorescence A change in the florescence from red to green indicates a decrease in the MMP Approximately 5×105/ml cells in 6-well plates were treated with various concentrations of curcumin for

24 h The cells were then washed with PBS and incubated with JC-1 working solution for 20 min at 37°C in the dark Cells were washed with PBS and resuspended in

500μl PBS The stained cells were analyzed by flow cyto-metry to determine the change in the florescence from red to green

Table 1 Characteristic of patients

P patient, Y year, M male, FAB French-American-British, WBC white blood cells, BMC bone marrow cells, BM bone marrow, PM peripheral blood.*Percentage of CD34 +

cells in bone marrow cells of AML patients before sorting #

The t (8; 21) (q22; q22) chromosomal translocation gives rise to the AML1/ETO fusion oncoprotein.

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RNA isolation and semiquantitative reverse

transcription-polymerase chain reaction (RT-PCR)

Total RNA was extracted using Trizol isolation reagent

(Invitrogen, USA) Reverse transcription was performed

using a reverse transcriptase first strand cDNA synthesis

kit (Takara, Japan) The sequences of the sense and

anti-sense primers were: 5’-CTGGTGGACAACATCGC-3’

(sense) and 5’-GGAGAAATCAAACAGAGGC-3’

(anti-sense) for Bcl-2, 5’-TGACTTTTCCTGTGAACTCT-3’

(sense) and 5’-GCCTTTCATTCGTATCAAGA-3’

(anti-sense) for c-IAP-1, 5’-GCAGGGTTTCT TTATACTG-3’

(sense) and 5’-TGTCCCTTCTGTTCTAACAG-3’

(anti-sense) for XIAP [32],

5’-GTGGACATCCGCAAAGAC-3’ (sense) and 5’-GAAAGGGTGTAA CGCAACT-5’-GTGGACATCCGCAAAGAC-3’

(anti-sense) forb-actin The PCR conditions were as

fol-lows: for c-IAP-1 and XIAP, 94°C for 1 min, 62°C for

1 min, and 72°C for 1 min; for Bcl-2, 94°C for 30 s,

62°C for 30 s, 72°C for 10 s; and for b-actin: 94°C for

30 s, 55°C for 30 s, 72°C for 1 min Thirty cycles of

amplification were used PCR (10μl) products were

ana-lyzed by electrophoresis on 2% (w/v) agarose gel

Western blot analysis

Total cellular proteins were isolated with lysis buffer

(20 mM Tris, pH 7.5; 150 mM NaCl; 0.25% NP40;

2.5 mM sodium pyprophosphate; 1 mM EGTA, 1 mM

EDTA; 1 mMb-glycerophosphate; 1 mM Na3VO4; 1 mM

PMSF; 1μg/ml leupeptin) Equal amounts of protein were

subjected to 10% or 15% sodium dodecyl

sulfate-polyacry-lamide gel electrophoresis and transferred to nitrocellulose

membranes The membranes were treated with primary

antibodies overnight at 4°C and incubated with a

HRP-conjugated anti-mouse or anti-rabbit secondary antibody

at room temperature for 1 h The protein bands were

visualized using an enhanced chemiluminescence reagent

(Pierce Biotechnology, USA), according to the

manufac-turer’s instructions

Short interfering RNA (siRNA) transfection

KG1a and Kasumi-1 cells were seeded onto 6-well plates

for 24 h before transfection Control scrambled siRNA

was synthesized and purchased from GenePharma

(Shang-hai Co Ltd., China) SiRNA Bcl-2 (50 nM):

5’-GGGA-GAUAGUGAUGAAG UAUU-3’ [33] or control scramble

sequences were transfected using Lipofectamine 2000

reagent (Invitrogen), according to the manufacturer’s

pro-tocol Briefly, for each well, 5μl Lipofectamine 2000 was

diluted in 250μl Opti-MEM medium (Invitrogen) The

mixture was gently added to a solution containing siRNA

in 250μl Opti-MEMI medium and incubated for 20 min

The mixture was then added to the plates After

transfec-tion with siRNA for 24 h, cells were harvested for further

assay

Statistical analysis Data were presented as mean ± SD One-way ANOVA fol-lowed by Bonferroni multiple comparison was performed

to assess the differences between two groups under multi-ple conditions If the data failed the normality test, the Kruskal-Wallis one-way ANOVA on ranks was used A value of p < 0.05 was considered statistically significant Both Calcusyn software (Biosoft, Ferguson, MO, USA) [34,35] and Jin’s formula [36] were used to evaluate the synergistic effects of drug combinations Jin’s formula is given as: Q = Ea + b/(Ea + Eb-Ea × Eb) Ea+b represents the cell proliferation inhibition rate of the combined drugs, while Ea and Eb represent the rates for each drug respectively A value of Q = 0.85-1.15 indicates a simple additive effect, while Q > 1.15 indicates synergism Combi-nation index (CI) plots were generated using CalcuSyn software A value of CI < 1 indicates synergism

Results

CD34+KG1a and Kasumi-1cells were insensitive to DNR KG1a, Kasumi-1 and U937 AML cells were stained with PE-conjugated CD34 antibody and subjected to flow cytometry to determine the purity of CD34+ cells The percentages of CD34+cells were 99.43 ± 0.60% in KG1a cells, 96.67 ± 0.11% in Kasumi-1 cells, but CD34+ was absent in U937 cells (Figure 1A) After treatment of these three cell lines with different concentrations of DNR for 48 h, MTT and apoptosis analyses showed that DNR inhibited proliferation and induced apoptosis in more mature U937 cells, but not in immature CD34+ KG1a or Kasumi-1 cell lines (Figure 1B, C) This was in accord with previous studies indicating that CD34+ AML cells were insensitive to DNR The concentration

of DNR used in this study was clinically achievable in patients [37,38]

Curcumin suppressed cell growth and induced G1/S cell cycle arrest in both DNR-insensitive and -sensitive AML cell lines

KG1a, Kasumi-1 and U937 cell lines were exposed to curcumin (0-100μM) for 24, 48, 72 and 96 h The cyto-toxic effects of curcumin were determined by MTT assay Curcumin had a significant cytotoxic effect in all tested cell lines in both dose- and time-dependent man-ners (Figure 2B, C, D) The IC50 values at 24, 48, 72, and 96 h were 230.5, 86.9, 60.0, and 35.7μM for KG1a, 68.5, 46.6, 28.8, and 23.5 μM for Kasumi-1, and 58.3, 26.0, 10.6, and 4.4μM for U937 cells, respectively The antiproliferative effects of curcumin in these cell lines were further determined using clonogenic assays Curcu-min inhibited clonogenic growth in a dose-dependent manner, and completely inhibited colony formation at a dose as low as 20μM (Figure S1A, B, Additional file 1)

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Cell cycle distributions in KG1a, Kasumi-1, and U937

cells were examined after treatment with curcumin for

24 h As shown in Figure 2E, treatment of KG1a cells

with 80μM curcumin resulted in a significant increase

in the percentage of cells in the G1 phase, from 46-62%,

and a decrease in the percentage of cells in the S phase, from 39-23% Similar results were found for Kasumi-1 and U937 cells These results demonstrated that curcu-min induced G1/S arrest in both DNR-insensitive and -sensitive AML cell lines

M1

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96.71

Daunorubicin(ȝg/ml)

Daunorubicin(ȝg/ml)

U937

C

Annexin č

PI

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1.65

8.13 0.02

90.19 1.35

10.15 0.00

88.50

4.84

0.89

94.27

0.00 0.37

2.69

26.94

0.00

1.32

4.65 0.01

94.02 0.69

3.64 0.00

95.67 0.42

3.51 0.00

96.07 0.56

3.69

0.05

95.70

14.16

26.56 12.68

46.60 12.39

16.13 48.40

23.08 8.78

19.60 1.62

69.99 0.64

2.75

0.01

96.60

Figure 1 CD34+KG1a and Kasumi-1cells were insensitive to DNR (A) KG1a, Kasumi-1 and U937 cells were stained with PE-conjugated CD34

antibody and subjected to flow cytometry to determine the purity of CD34+cells (B, C) These three cell lines were treated with different

concentrations of DNR for 48 h MTT assay (B) was performed as described in “Methods” and apoptosis (C) was assessed by Annexin V/PI assays.

Cells in the lower right quadrant represent early apoptosis and those in the upper right quadrant represent late apoptosis The graph displays

the means ± SD of three independent experiments * p < 0.05, ** p < 0.01, *** p < 0.001 (compared with control).

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KG1a Kasumi-1 U937

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Curcumin(ȝM)

U937

Figure 2 Curcumin suppressed cell growth and induced G1/S arrest (A) Structure of curcumin (B, C, D) KG1a, Kasumi-1 and U937 cell lines were treated with different concentrations of curcumin for 24, 48, 72, and 96 h MTT assay was performed (E) These three cell lines were treated with different concentrations of curcumin for 24 h and analyzed for DNA content by flow cytometry, as described in “Methods.” The bar represents means ± SD of three independent experiments.

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Curcumin induced apoptosis through activation of

caspase-3 followed by PARP degradation in both

DNR-insensitive and -sensitive AML cell lines

To determine if growth inhibition induced by curcumin

was a result of apoptosis, the pro-apoptotic effect was

examined using Wright-Giemsa, Hoechst 33342 and

Annexin-V/PI staining Both Wright-Giemsa and

Hoechst 33342 staining showed that curcumin induced

morphological changes such as cell shrinkage and nuclear

condensation, which are typical characteristics of

apopto-sis (Figure 3A; Figure S2A, Additional file 2) These

mor-phological changes were confirmed by flow cytometry

Treatment with curcumin at 40μM for 24 h resulted in

apoptosis rates of 23.5 ± 8.8%, 36.1 ± 5.3%, and 40.1 ±

17.8% in KG1a, Kasumi-1 and U937 cells, respectively

(Figure 3B) Western blotting analysis further showed

that curcumin induced caspase-3 activation and PARP

cleavage, two hallmarks of apoptosis (Figure 3C) Both

Annexin-V/PI and Western blotting showed that

curcu-min induced apoptosis in a dose-dependent manner

U937cells were the most sensitive to curcumin-induced

apoptosis, followed by Kasumi-1, then KG1a cells

Curcumin decreased Bcl-2 mRNA and protein levels and

reduced MMP in both DNR-insensitive and -sensitive AML

cell lines

The mechanisms underlying curcumin-induced

apopto-sis were investigated The IAP and Bcl-2 family play an

important role in the regulation of cell apoptosis, and

the effects of curcumin on mRNA levels of c-IAP-1,

XIAP and Bcl-2 were therefore assessed by RT-PCR As

shown in Figure 4A, Bcl-2 mRNA levels were

signifi-cantly down-regulated in both DNR-insensitive AML

cell lines (KG1a and Kasumi-1) and in DNR-sensitive

U937 cells, while the levels of c-IAP-1 and XIAP were

unchanged Western blotting also demonstrated that

curcumin significantly down-regulated Bcl-2 protein

levels in a dose-dependent manner (Figure 4B) These

results suggest that down-regulation of Bcl-2 could

con-tribute to curcumin-induced apoptosis

Disruption of the function of Bcl-2 protein leads to

per-meabilization of the mitochondrial membrane [39] We

therefore investigated the effects of curcumin on MMP

using JC-1 fluorescent dye and flow cytometry Exposure

of the three cell lines to increasing doses of curcumin for

24 h led to a significant reduction in the MMP (Figure

4C) These results suggest that curcumin-induced

apopto-sis is mitochondria-dependent

Curcumin synergistically enhanced the cytotoxic effect of

DNR in DNR-insensitive KG1a and Kasumi-1 cells,

associated with down-regulation of Bcl-2

To determine if curcumin could enhance the cytotoxic

activity of DNR, DNR-insensitive KG1a and Kasumi-1

cells were cultured with combinations of these two drugs at different doses but in a constant ratio (curcu-min to DNR: 20 μM to 0.1 μg/ml, 40 μM to 0.2 μg/ml, and 80 μM to 0.4 μg/ml, respectively) for 48 h, as shown in Figure 5A, B and Table S1 (Additional file 3) Both CalcuSyn software and Jin’s formula were used to determine synergy, and the results were consistent With the exception of co-treatment of KG1a cells with

20μM curcumin and 0.1 μg/ml DNR, which showed an additive effect (CI = 1.03, Q = 0.99), co-treatment with other doses in KG1a cells and with all doses in

Kasumi-1 cells exhibited synergistic effects For example, the combination of 40μM curcumin with 0.2 μg/ml DNR

in KG1a cells caused growth inhibition of 45.12%, com-pared to curcumin (26.31%) or DNR (5.47%) alone, indi-cating synergism (CI = 0.654, Q = 1.49) Notably, co-treatment with 40 μM curcumin and 0.2 μg/ml DNR caused more attenuation of Bcl-2 protein levels than treatment with either agent alone (Figure 5C)

Suppression of Bcl-2 with siRNA induced apoptosis and increased the susceptibility of KG1a and Kasumi-1 cells to DNR-induced apoptosis

To clarify if down-regulation of Bcl-2 by curcumin plays

an important role in this synergistic effect, Bcl-2 expres-sion was suppressed by siRNA and the effect on apopto-sis and DNR sensitivity was examined by flow cytometry Bcl-2 siRNA-induced apoptosis in 24 h (28.58% in KG1a cells, 37.12% in Kasumi-1 cells) was similar to that in cur-cumin-treated KG1a (31.71%, 60 μM, Figure 3B) and Kasumi-1 cells (36.10%, 40μM, Figure 3B), respectively (Figure 6A, B) As shown in Figure 6C, suppression of Bcl-2 by siRNA increased the susceptibility of these cell lines to DNR-induced apoptosis (40.15% in KG1a cells and 86.23% in Kasumi-1 cells), compared to DNR only (3.17% in KG1a cells, 5.94% in Kasumi-1 cells) These results suggest that suppression of Bcl-2 could contribute

to curcumin-induced apoptosis and the synergistic effect

of curcumin and DNR

Curcumin was effective against primary CD34+AML cells The cytotoxic effects of either curcumin and/or DNR on primary CD34+AML cells were also examined CD34+ cells were sorted from BMMCs or PBMCs from 9 AML patients and 8 healthy donors The sorted samples yielded more than 95% CD34+cells with greater than 90% viabi-lity, determined by trypan blue exclusion (Figure 7A) The antiproliferative effects of curcumin on CD34+cells from

3 AML patients (patients 1, 2, 3) and 3 healthy donors (donors 1, 2, 3) were determined by MTT assay, and com-pared with the results of DNR treatment CD34+ cells were treated with curcumin (0, 10, 20, 40, 80μM) or DNR (0, 0.4, 0.8, 1.6μg/ml) for 24 h Curcumin significantly inhibited proliferation of CD34+AML cells, but only

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0 40 60 80 0 40 60 80 0 40 60 80

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Cleaved PARP

GAPDH Curcumin(ȝM) Annexin č

PI

B

Curcumin(ȝM) 0.26

91.83

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5.55

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Figure 3 Curcumin induced apoptosis through activation of caspase-3 followed by PARP degradation KG1a, Kasumi-1 and U937 cells were incubated with indicated concentrations of curcumin for 24 h (A) Cells were stained with Wright-Giemsa and then examined under a light microscope Arrows indicate apoptotic cells (magnification ×400) (B) Cells were stained with Annexin V/PI to analyze apoptotic cell

populations The graph displays the means ± SD of four independent experiments (C) Western blotting analysis showed cleaved caspase-3 (17,

19 kDa) and cleaved PARP (89 kDa) fragment Three independent experiments were performed with similar results, and representative data are shown.

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C

Curcumin(ȝM)

Curcumin(ȝM)

GAPDH Bcl-2

0 40 60 80 0 40 60 80

KG1a kasumi-1 U937

Curcumin(ȝM)

0 40 60 80

Green Red

Curcumin(ȝM)

38.27 19.14

80.82 23.86

76.13 37.65

62.33 93.25

6.47

49.91 97.31

50.05 72.29

27.68 92.88

7.08 2.58

0.36

99.63 7.25

92.74 20.25

79.73 84.76

15.22

Figure 4 Curcumin decreased Bcl-2 mRNA and protein levels and caused the loss of MMP KG1a, Kasumi-1 and U937 cells were exposed

to different concentrations of curcumin for 24 h (A) The effects on Bcl-2, c-IAP-1, and XIAP mRNA levels were determined by RT-PCR (B) The effect on Bcl-2 protein levels was determined by Western blotting assay Three independent experiments were performed with similar results, and representative data are shown (C) MMP was estimated by flow cytometry showing decrease in the red to green fluorescence ratio The results shown are representative of three independent experiments The bar represents mean ± SD of three independent experiments.

Trang 10

Bcl-2 GAPDH

– + – +

KG1a Kasumi-1

Daunorubicin(0.2ȝg/ml) Curcumin(40ȝM)

C

A

c

a

b

a

KG1a

B

Figure 5 Curcumin synergistically enhanced the cytotoxic effects of DNR associated with down-regulation of Bcl-2 KG1a and Kausumi-1cells were exposed to different concentrations of curcumin, DNR, or their combination as indicated, for 48 h (A, B) CI-effect plots and median-effect plots were generated using CalcuSyn software The points a, b, and c represent CI values for the combinations 20, 40, and 80 μM

curcumin with 0.1, 0.2, and 0.4 μg/ml DNR in a constant ratio, respectively The CI values at ED 50 , ED 75 , ED 90 were 0.667, 0.490, and 0.364 for KG1a cells and 0.529, 0.456, and 0.394 for Kasumi-1 cells, respectively (C) Bcl-2 protein levels were determined by Western blotting assay Three independent experiments were performed with similar results, and representative data are shown.

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